TOMOYUKI MAKINO, ATSUSHI MIZOKAMI and MIKIO NAMIKI

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1 Clinical Outcomes of Patients with Localized and Locally Advanced Prostate Cancer Undergoing High-dose-rate Brachytherapy with External-beam Radiotherapy at our Institute TOMOYUKI MAKINO, ATSUSHI MIZOKAMI and MIKIO NAMIKI Department of Integrative Cancer Therapy and Urology, Kanazawa University Graduate School of Medical Science, Kanazawa, Ishikawa, Japan Abstract. Aim: To report the clinical outcomes of localized and locally advanced prostate cancer patients undergoing high-dose-rate brachytherapy (HDR-BT) with external-beam radiotherapy (HDR-BT+EBRT) at the Kanazawa University Hospital. Patients and Methods: From 1999 until 2012, we examined 327 patients with T1c-T3bN0M0 prostate cancer that underwent HDR-BT+EBRT and were followed-up for 1 year. Before 2005, treatment consisted of HDR-BT at 18 Gy/3 fractions and EBRT to the prostate at 44 Gy/22 fractions, whereas after 2006, treatment consisted of HDR- BT at 19 Gy/2 fractions and EBRT to the prostate at 46 Gy/23 fractions. Results: Median age was 68 years (range=45-84 years), median follow-up duration was 57 months (range= months), and median prostatespecific antigen (PSA) level at diagnosis was 9.2 ng/ml (range= ng/ml). The patients clinical stages were T1c:82, T2a:112, T2b:70, T2c:5, T3a:29, T3b:29, and their Gleason score was 6:120, 7:108, 8:99, respectively. The 5-year overall survival, and biochemical recurrence-free survival (brfs) was 97.5% and 95.3%, respectively. Recurrence was reported in 20 cases (6.1%), and 11 patients died during follow-up, but only 1 patient died of prostate cancer. The 5-year recurrence-free survival brfs for the patients in low-risk, intermediate-risk, and high-risk groups according to the D Amico risk classification criteria were 100%, 95.6%, and 90.7%, respectively. Regarding adverse events genitourinary toxicity was major, and thus, 8.8% patients had urethral stricture and 4.3% patients were classified as grade 3. Conclusion: HDR-BT+EBRT is Correspondence to: Dr. Tomoyuki Makino, Department of Integrative Cancer Therapy and Urology, Kanazawa University Graduate School of Medical Science, Kanazawa, Ishikawa, Japan. mackeeen511@gmail.com Key Words: Prostate cancer, high-dose-rate brachytherapy. considered a suitable treatment modality for localized and locally advanced prostate cancer, including high-risk cases. However, genitourinary toxicity is observed frequently, and therefore, it may be necessary to modify the therapeutic planning of the HDR-BT+EBRT modality. Current strategies for localized prostate cancer (PCa) are radical prostatectomy (RP), hormonal therapy (HT), and radiotherapy (RT). Although treatment outcomes of RP for localized early-stage PCa are good, the procedure has several disadvantages. This therapy is more invasive than other forms of therapies, biochemical recurrence-free survival (brfs) decreases in high-risk patients (1, 2), and there is a high incidence of adverse effects, such as urinary incontinence and erectile dysfunction (3, 4). In contrast, HT is well-tolerated, and many patients of advanced age can undergo this therapy. However, HT is also associated with a number of adverse effects, such as erectile dysfunction, hot flashes, and osteoporosis (5-7). In addition, outcomes of HT are poorer than those of RP and RT (8). High-dose-rate brachytherapy (HDR-BT) is an effective treatment modality that can be utilized either alone or in combination with external-beam RT (EBRT) for patients with localized PCa in all risk groups (9-12). Combined use of EBRT and HDR-BT allows for considerable dose escalations while decreasing the dose administered to organs at risk, thereby improving PCa treatment outcomes (13). Furthermore, it has been reported that the combination of androgen deprivation therapy (ADT) with EBRT and HDR-BT improved treatment results of highrisk PCa cases (14). We have previously reported the usefulness of HDR-BT with EBRT (15). We have treated 446 patients between February 1999 and December 2012 at the Kanazawa University Hospital. We could accumulate a number of cases, and conduct a long follow-up schedule. In the present study, we performed an updated analysis of the outcomes of the HDR-BT with EBRT treatment to examine its usefulness. In /2015 $

2 addition, we examined a utility of the combination of ADT with HDR-BT and EBRT. Patients and Methods In our institution, HDR-BT was indicated for non-metastasized PCa cases of any T stage. The present study population consisted of 327 patients diagnosed with T1c-T3bN0M0 PCa who were followed up for 1 year. In this study, we described T1c-T3bN0M0 PCa as localized and locally advanced PCa. Lesions were categorized according to the tumor-node-metastasis classification by the International Union Against Cancer (2009). Risk classification was based on that developed by D Amico (16), by which patients were classified as having low risk (PSA 10 ng/ml, Gleason score 6, and clinical stage T2a), intermediate risk (PSA ng/ml and/or Gleason score=7 and/or clinical stage T2b), and high risk (PSA 20 ng/ml and/or Gleason score 8 and/or clinical stage T2c). Neoadjuvant HT (NAHT) was administered to decrease the prostate volume (<30 ml) and prevent disease progression while awaiting treatment. Adjuvant HT (AHT) for 2-3 years was recommended for high-risk patients. HT consisted basically of luteinizing hormone-releasing hormone agonist with or without bicalutamide. The HDR-BT treatment strategy consisted of using an 192Ir microselectron (Nucletron, BV, Leersum, Holland) at 18 Gy/3 fractions and EBRT to the prostate at 44 Gy/22 fractions between 1999 and 2005, whereas HDR-BT at 19 Gy/2 fractions and EBRT to the prostate at 46 Gy/23 fractions was used after In this study, biochemical recurrence was determined according to the Phoenix criteria (17). The survival curves were calculated by the Kaplan-Meier method. Adverse effects were recorded according to the Common Terminology Criteria for Adverse Events v4.0. Results Patients characteristics are shown in Table I. The mean patient age was 67.6 years (range=45-84 years) and the median follow-up duration was 57.5 months (range, months). Of the 327 patients included in this study, 82 (25.1%) were in clinical stage T1c, 112 (34.2%) in T2a, 70 (21.4%) in T2b, 5 (1.5%) in T2c, 29 (8.9%) in T3a, and 29 (8.9%) in T3b. The median initial PSA level was 9.2 ng/ml (range= ng/ml) and the Gleason score was 6 (120, 36.7%), 7 (108, 33%), 8 (99, 30.3%). According to the D Amico risk classification criteria, 69 patients were at low risk, 118 were at intermediate risk, and 140 were at high risk. A total of 286 patients (87.5%) underwent NAHT for a median of 6 months. Seventy-eight patients (23.9%) received AHT for a mean of 2.4 years. Patients in the AHT group were mainly high-risk subjects (69, 88.5%). Figure 1 shows the various survival curves calculated by the Kaplan-Meier method. The 5-year and 8-year overall survival (OS) was 97.5% and 93.1%, respectively (Figure 1A). The 5-year and 8-year brfs rates were 95.3% and 89.6%, respectively. The 5-year brfs for the patients in lowrisk, intermediate-risk, and high-risk group was 100%, 95.6%, and 90.7%, respectively (Figure 1B). When limited to the non-aht group, the 5-year brfs for patients in the Table I. Characteristics of the patients (T1c-T3b, N0, M0). Mean age (years) 67.6 (45-84) N=327 Follow-up (months) Median 57.5 (12-148) Mean 61.2 Clinical stage T1c 82 T2a 112 T2b 70 T2c 5 T3a 29 T3b 29 Gleason score PSA at diagnosis Median 9.2 ( ) ng/ml Mean 17.5 ng/ml Neoadjuvant hormone therapy 41 Adjuvant hormone + 78 therapy 249 D Amico risk Low 69 classification* Intermediate 118 High 140 *Low risk: PSA 10 and Gleason score 6 and clinical stage T2a. Intermediate risk: PSA10-20 and/or Gleason score=7 and/or clinical stage T2b. High risk: PSA 20 and/or Gleason score 8 and/or clinical stage T2c. low-risk, intermediate-risk, and high-risk groups was 100%, 95.4%, and 87.6%, respectively (Figure 1C). One patient died of prostate cancer. Table II shows the characteristics of patient recurrence. Eight out of 140 patients (5.7%) presented recurrence in the high-risk group and 12 out of 187 patients (6.4%) in the lowrisk/intermediate-risk groups (low: 5 patients, intermediate: 7 patients). Table III shows the characteristics of high-risk patients. AHT was administered in approximately half of the cases. Biochemical recurrence was observed in 5 patients (7.0%) in the non-aht group and in 3 patients (4.3%) in the AHT group. Figure 2 shows brfs curves for high-risk patients. The 5-year brfs was 93.6% and 87.6% in the AHT and the non-aht groups, respectively. Although there was no significant difference in the recurrence rate between non- AHT and AHT groups, there were more patients with 2-3 risk factors according to the D Amico risk classification in the AHT group than in the non-aht group. Adverse events were observed in 73 patients (Table IV). The most frequent genitourinary complications were pollakiuria or urgency (10.4%) without grade 3 toxicity. Urethral stricture was found in 8.8% cases and 4.3% of them were grade 3, which were observed in the late phases (median=638 days; range= days) and managed 1724

3 Makino et al: Outcomes of PCa Patients Undergoing HDR-BT plus ERBT Figure 2. Recurrence-free survival rate of 140 high-risk patients stratified by whether AHT was performed or not. successfully by urethral dilatation or internal urethrotomy. In contrast, rectal toxicity, such as proctitis, diarrhea, and rectal hemorrhage, was rare. Most of them were grade 2 at a rate of <1%, but only 1 patient experienced grade 3 rectal hemorrhage. Discussion Figure 1. A. Overall survival and recurrence-free survival rates for all patients. B. Recurrence-free survival rates for all patients stratified by the risk group. C. Recurrence-free survival rate for non-aht group stratified by the risk group. Over the past years, many institutions have reported on treatment outcomes of HDR-BT for patients with PCa. The 5-year brfs for patients in the low-risk, intermediate-risk, and high-risk groups in most reports was 90%, 80%-90%, 60%-70%, respectively (14). According to our study, the 5- year brfs for patients in the low-risk, intermediate-risk, and high-risk groups was 100%, 95.6%, and 90.7%, respectively. These promising results can be explained by the combined use of HT, although the irradiation dose employed was lower than in previous studies. In the present work, NAHT was administered in 286 patients (87%) and AHT was administered in 78 patients (24%). AHT was administered in 69 patients of the high-risk group, which corresponded to approximately half of the patients in this group. The 5-year brfs of the high-risk non-aht and AHT groups was 87.6% and 93.6% (p = 0.49). When we compared the non-aht groups with the AHT groups in the high-risk group, the mean PSA level was 13.6 ng/ml and 45.5 ng/ml, respectively. Furthernore, there were more patients with 2 risk factors according to the D Amico risk classification, and with higher T stages, such as ct3, in the AHT group. In other words, the patients at higher risk became part of the AHT groups. The dosing period of AHT had a mean of 2.4 years, which corresponds to the recommended dosing period according to the NCCN guidelines (2-3 years). After all, HT is considered 1725

4 Table II. Characteristics of patients recurrence. Subgroup (No. of patients recurrence) Mean age T-stage Gleason score PSA Number of high risk factor High group 8(/140: 5.7%) 65.5 T1c: 1 6:1 Mean: factor: 7 (/85: 8.2%) T2a: 3 7:1 10:4 2 factors: 1 (/29: 3.4%) T2b: 2 8: :3 3 factors: 0 (/26: 0%) T3a: 2 20:1 Low/Intermediate group 12(/187: 6.4%) 69.4 T1c: 6 6:7 Mean: 6.3/11.3 Classification: T2a: 1 7:5 Low 5(/69:7.2%) T2b: 5 Intermediate 7(/118: 5.9%) Table III. Characteristics of high risk patients. Subgroup (No. of patients) Mean age T-stage Gleason score PSA Number of high risk factor PSA recurrence AHT( ) group (n=71) 67.4 T1c: 15 6:6 Mean: factor: 63 5 (7.0%) T2a: 27 7:16 10:41 2 factors: 8 1 factor: 5 T2b: 13 8: :16 3 factors: 0 2 factors: 0 T2c: 3 20:14 T3a: 10 T3b: 3 AHT(+) group (n=69) 68.5 T1c:1 6:4 Mean: factor: 22 3 (4.3%) T2a: 5 7:15 10:11 2 factors: 21 1 factor: 2 T2b: 16 8: :13 3 factors: 26 2 factors: 1 T2c: 2 20:45 T3a: 19 T3b: 26 more effective in cases in which distant micrometastasis are thought to be present by the time of primary therapy. The Radiation Therapy Oncology Group Protocol (RTOG 92-02) was a randomized trial comparing the use of shortterm vs. long-term AHT combined with EBRT for patients with T2c-T4 locally advanced (18). Statistically significant improvement in biochemically disease control, distant metastasis failure, local control, and disease-free survival were observed for patients receiving long-term HT. Thus, these results suggest that long-term AHT is at least effective for higher-risk patients. However, we have to consider the possibility that AHT will maintain serum testosterone levels low for extended periods of time, even after discontinuing HT because of testicular atrophy. A persistent low testosterone level may prevent PCa recurrence. Likewise, the incidence of recurrence may increase after serum testosterone level increases. Therefore, we need to observe patients, who underwent AHT, carefully for a long term. In our study, the adverse events were mainly genitourinary toxicities, such as urethral stricture and pollakiuria or urgency. Several studies have reported cases of urethral stricture following HDR-BT with EBRT, with a urethral stricture rate of 5%-10%. Strictures were located at the Table IV. Adverse events. All grades Grade 3 (n=73) Urethral stricture 29 (8.8%) 14 (4.3%) Pollakisuria, urgency 34 (10.4%) Urinary retention 2 (0.6%) Hematuria 3 (0.9%) Acute prostatitis 2 (0.6%) Diarrhea 3 (0.9%) Proctitis 3 (0.9%) Rectal hemorrhage 2 (0.6%) 1 (0.3%) bulbo-membranous urethra in 92.1% cases, with a median time to diagnosis of 22 months (19-24 months). Urethral stricture in our study occurred at similar rates as those described in previous studies. Therefore, surgical management, such as dilatation and internal urethrotomy, was necessary for approximately half of the patients. The HDR-BT modality dose has certain limitations. For instance, the patients require complete bed resting during the treatment period to avoid the accidental removal of the 1726

5 Makino et al: Outcomes of PCa Patients Undergoing HDR-BT plus ERBT catheter from the perineum. Therefore, this aspect is less convenient for patients. In addition, this method is associated with an increased risk of deep vein thrombosis. In contrast, it has been reported that the administration of a single-fraction HDR protocol resulted in a high disease control rate and low toxicity (25). Therefore, this modality may contribute to a short treatment time and improve of the quality of life of patients during the treatment course. We recently began administering the single-fraction HDR protocol, but a longer follow-up is required to assess the effect of this dose escalation protocol on long-term biological control. There has been no randomized trial of the combination of ADT and HDR-BT. Further study is required to explore whether ADT really improves OS when it is combined with HDR-BT. Conclusion Herein, we report an updated analysis of the outcomes of PCa patients treated with HDR-BT+EBRT. We obtained good results, even in the high-risk cases. Especially, longterm AHT for patients at very high-risk might be appropriate. However, urethral stricture seems an unavoidable reaction. Thus, the HDR protocol still offers some room for improvement. HDR-BT+EBRT was considered a good strategy for localized and locally advanced PCa. In addition, tri-modality treatment of the combination of ADT may contribute to improvement of OS. Although further studies with longer follow-up are necessary. References 1 D'Amico AV, Whittington R, Malkowicz SB, Weinstein M, Tomaszewski JE, Schultz D, Rhude M, Rocha S, Wein A and Richie JP: Predicting prostate specific antigen outcome preoperatively in the prostate specific antigen era. J Urol 166: , Hull GW, Rabbani F, Abbas F, Wheeler TM, Kattan MW and Scardino PT: Cancer control with radical prostatectomy alone in 1,000 consecutive patients. J Urol 167: , Dubbelman YD, Dohle GR and Schroder FH: Sexual function before and after radical retropubic prostatectomy: a systematic review of prognostic indicators for a successful outcome. Eur Urol 50: , Frank SJ, Pisters LL, Davis J, Lee AK, Bassett R and Kuban DA: An assessment of quality of life following radical prostatectomy, high dose external beam radiation therapy and brachytherapy iodine implantation as monotherapies for localized prostate cancer. J Urol 177: , Thompson CA, Shanafelt TD and Loprinzi CL: Andropause: symptom management for prostate cancer patients treated with hormonal ablation. Oncologist 8: , Joly F, Alibhai SM, Galica J, Park A, Yi QL, Wagner L and Tannock IF: Impact of androgen deprivation therapy on physical and cognitive function, as well as quality of life of patients with nonmetastatic prostate cancer. J Urol 176: , Kumar RJ, Barqawi A and Crawford ED: Preventing and treating the complications of hormone therapy. Curr Urol Rep 6: , Akaza H, Homma Y, Usami M, Hirao Y, Tsushima T, Okada K, Yokoyama M, Ohashi Y, Aso Y; Prostate Cancer Study Group: Efficacy of primary hormone therapy for localized or locally advanced prostate cancer: results of a 10-year follow-up. BJU Int 9: , Forsythe K, Burri R, Stone N and Stock RG: Predictors of metastatic disease after prostate brachytherapy. Int J Radiat Oncol Biol Phys 83: , Stone NN, Potters L, Davis BJ, Ciezki JP, Zelefsky MJ, Roach M, Shinohara K, Fearn PA, Kattan MW and Stock RG: Multicenter analysis of effect of high biologic effective dose on biochemical failure and survival outcomes in patients with Gleason score 7-10 prostate cancer treated with permanent prostate brachytherapy. Int J Radiat Oncol Biol Phys 73: , Potters L, Morgenstern C, Calugaru E, Fearn P, Jassal A, Presser J and Mullen E: 12-Year outcomes following permanent prostate brachytherapy in patients with clinically localized prostate cancer. J Urol 173: , Blasko JC, Grimm PD, Sylsvester JE and Cavanagh W: The role of external beam radiotherapy with I-125/Pd-103 brachytherapy for prostate carcinoma. Radiother Oncol 57: , Deutsch I, Zelefsky MJ, Zhang Z, Mo Q, Zaider M, Cohen G, Cahlon O and Yamada Y: Comparison of PSA relapse free survival in patients treated with ultra-high-dose IMRT versus combination HDR brachytherapy and IMRT. Brachytherapy 9: , Ishiyama H, Satoh T, Kitano M, Tabata K, Komori S, Ikeda M, Soda I, Kurosaka S, Sekiguchi A, Kimura M, Kawakami S, Iwamura M and Hayakawa K: High-dose-rate brachytherapy and hypofractionated external beam radiotherapy combined with long-term hormonal therapy for high-risk and very high-risk prostate cancer: outcomes after 5-year follow-up. Journal of Radiation Research. J Radiat Res 55: , Takahiro Nohara, Atsushi Mizokami, Tomoyasu Kumano, Kazuyoshi Shigehara, Hiroyuki Konaka, Kadono Yoshifumi, Kitagawa Yasuhide, Kouji Izumi, Kazutaka Narimoto and Mikio Namiki: Clinical Results of Iridium-192 High Dose Rate Brachytherapy with External Beam Radiotherapy. Jpn J Clin Oncol 40: , D Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K,Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ and Wein A: Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280: , Roach M 3rd, Hanks G, Thames H Jr, Schellhammer P, Shipley WU, Sokol GH and Sandler H: Defining biochemical failure following radiotherapy with or without hormonal therapy in men with clinically localized prostate cancer: recommendations of the RTOG-ASTRO Phoenix Consensus Conference. 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6 19 Sullivan L, Williams SG, Tai KH, Foroudi F, Cleeve L and Duchesne GM: Urethral stricture following high dose rate brachytherapy for prostate cancer. Radiother Oncol 91: , Borghede G, Hedelin H, Holmang S, Johansson KA, Sernbo G and Mercke C: Irradiation of localized prostatic carcinoma with a combination of high dose rate iridium-192 brachytherapy and external beam radiotherapy with three target definitions and dose levels inside the prostate gland.radiother Oncol 44: , Mate TP, Gottesman JE, Hatton J, Gribble M and Van Hollebeke L: High dose rate afterloading 192Iridium prostate brachytherapy: feasibility report. Int J Radiat Oncol Biol Phys 41: , Curran MJ, Healey GA, Bihrle W 3rd, Goodman N and Roth RA: Treatment of high-grade low-stage prostate cancer by highdose-rate brachytherapy. J Endourol 14: , Martinez A, Gonzalez J, Spencer W, Gustafson G, Kestin L, Kearney D and Vicini FA: Conformal high dose rate brachytherapy improves biochemical control and cause specific survival in patients with prostate cancer and poor prognostic factors. J Urol 169: , Demanes DJ, Rodriguez RR, Schour L, Brandt D and Altieri G: High-dose-rate intensity-modulated brachytherapy with external beam radiotherapy for prostate cancer:california endocurietherapy s 10-year results. Int J Radiat Oncol Biol Phys 61: , Morton G, Loblaw A, Cheung P, Szumacher E, Chahal M, Danjoux C, Chung HT, Deabreu A, Mamedov A, Zhang L, Sankreacha R, Vigneault E and Springer C: Is single fraction 15 Gy the preferred high dose-rate brachytherapy boost dose for prostate cancer? Radiother Oncol 100: , Received June 6, 2014 Revised August 19, 2014 Accepted August 25,

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